Humble Shrub Sheds Light on History of Flowering Plants

Amborella is the duck-billed platypus of flowering plants. Like the bizarre, beaver-tailed creature, which represents the earliest branch of mammals, the large shrub with off-white flowers sits on the lowest branch of the flowering plants’ family tree. And just as the genome of the platypus helped researchers figure out what the first mammalian genomes looked like, the newly published sequence of Amborella points to an ancestor that was actually fairly sophisticated genetically. By comparing this plant’s DNA with other plant genomes, researchers are getting a stronger sense of how flowering plants came to dominate Earth.

“This is a highly significant step in terms of sorting out what happened early in evolution and what happened later,” says Michael Donoghue, an evolutionary biologist at Yale University, who was not involved in the research.

Flowering plants, also called angiosperms, arose at least 160 million years ago and quickly spread; today, they number more than 300,000 species that adorn the landscape and feed the world. When Charles Darwin looked at the fossil record, he was amazed at how many different kinds of angiosperms evolved so quickly, calling this burst “an abominable mystery.”

Knowing that the Amborella genome would provide clues about this puzzle, a large consortium has sequenced its DNA and compared that sequence to the DNA of almost two dozen other plants. Among Amborella’s 800 million DNA-building blocks, called bases, the researchers found evidence that the whole genome had duplicated sometime in the past, doubling the number of genes and the genome size. They discovered evidence of this duplication in other flowering plants, but not in conifers and other gymnosperms, which produce seeds but no flowers and preceded the evolution of flowering plants. This whole genome duplication event probably occurred in the ancestor to all angiosperms, about 240 million years ago, the Amborella Genome Project reports today in Science.

This ancestor “started off with a whole new set of duplicate genes,” says Michael Clegg, a plant geneticist at the University California, Irvine, who was not involved with the work. “The duplicated genes can take on a novel function.” Indeed, the genome comparisons revealed that angiosperms evolved 1179 novel genes, many of which gave rise to additional related genes to make up whole new gene families, says project co-leader Claude dePamphilis, an evolutionary biologist at Pennsylvania State University, University Park. Two new genes, for example, allow for the formation of water-conducting cells called vessel elements that are not found in nonflowering seed plants.

The data also indicate that the ancestral angiosperm had the basic portfolio of genes to make flowers, including 21 MADS-box genes that help determine what flower part—such as a petal or a stamen—forms where. But Amborella, which came later, has more: 36 MADS-box genes, and other flowering plants, which have undergone more whole genome duplications, have even more still, the researchers report. They think these additional genes paved the way for colorful and more structured and shapely flowers in later evolving angiosperms.

Several of the insights from the analysis of the whole genome confirm what researchers had thought. But the mitochondrial genome—five chromosomes that exist in the mitochondria separate from the DNA in the nucleus—held a big surprise. Its 3.8 million bases include the complete mitochondrial genomes of three green algae and one moss, as well as genes from other plants, evolutionary biologist Jeffrey Palmer of Indiana University, Bloomington, and his colleagues report today in another paper in Science. A few other plants have big mitochondrial genomes—Amborella’s is six times the typical size—but none have so much foreign DNA. Palmer says that makes Amborella one of the most extreme cases of horizontal gene transfer, a process in which one species takes on genes of another species. Most of those foreign genes don’t do anything, having degenerated into pseudogenes.

No one knows why Amborella is such a genome glutton. Amborella lives naturally only in New Caledonia, in a moist environment, with a lot of lichens and other organisms growing on its surfaces. When wounded, the plant sends out suckers that may take up foreign mitochondria, which may subsequently fuse with its own mitochondria, Palmer suggests.

“If this proposed mechanism is true, we should be seeing this in other plants,” Donoghue says, because many plants share close quarters with mosses and lichens and have similar wound responses. Other plants might assimilate other genomes frequently but quickly get rid of the extra DNA, whereas Amborella just hangs on to it. Palmer accepts that explanation, calling Amborella a “constipated glutton.” But the bottom line, says evolutionary biologist Erika Edwards of Brown University, is that “to document these whole genome insertions is really fantastic.”